Gustatory cortex of primates: anatomy and physiology

doi:10.1016/0168-0102(94)90017-5

Neuroscience Research

Volume 20, Issue 1, July 1994, Pages 1-13

https://doi.org/10.1016/0168-0102(94)90017-5 Get rights and content

Abstract

Clinical and physiological studies of patients with ageusia or gustatory hallucination suggest that the primary gustatory area (area G) lies at the anterior insula or at the base of the central sulcus. However, physiological and anatomical studies in subhuman primates, e.g. squirrel monkeys or macaque monkeys, locate area G at the buried frontal operculum (Fop) and dorsal insula. The presence of secondary or higher gustatory areas are claimed because taste neurons are found in the precentral opercular area (PrCO) or orbitofrontal cortex in alert monkeys. Part of the anterior insula is suggested to subserve the interface between area G and the amygdala. Many physiological studies have been conducted lacking knowledge of the histological boundaries of the primary and secondary gustatory areas. Some difference has been found in the physiological properties of taste neurons in the primary and secondary gustatory areas: the primary gustatory area contains various categories of taste neurons, whereas most of the taste neurons in the secondary gustatory areas (e.g., PrCO, area 1–2) are specifically sensitive to one of the four basic tastes, and taste neurons in the orbitofrontal opercular area (OFO), another secondary gustatory area, show sensory-specific hunger as well.

References (91)

L.L. Baylis et al.
Responses of neurons in the primate taste cortex to glutamate
Physiol. Behav.
(1991)
R.M. Benjamin
Some thalamic and cortical mechanisms of taste
R.M. Benjamin et al.
Projection of taste nerve afferents to anterior opercular-insular cortex in squirrel monkey (Saimiri sciureus)
Brain Res.
(1968)
R.M. Benjamin et al.
Projections of tongue nerve afferents to somatic sensory area I in squirrel monkey (Saimiri sciureus)
Brain Res.
(1968)
S. Ito et al.
Cytochrome oxidase staining facilitates unequivocal visualization of primary gustatory area in the fronto-operculo-insular cortex of macaque monkeys
Neurosci. Lett.
(1991)
M. Matelli et al.
Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey
Behav. Brain Res.
(1985)
H. Nishijo et al.
Topographic distribution of modality-specific amygdalar neurons in alert monkeys
J. Neurosci.
(1988)
H. Ogawa et al.
Oral cavity representation at the frontal operculum of macaque monkeys
Neurosci. Res.
(1989)
H. Ogawa et al.
Taste area in granular and dysgranular insular cortices in the rat identified by stimulation of the entire oral cavity
Neurosci. Res.
(1990)
M. Ohgushi et al.
Effects of iv angiotensin II on cortical neurons during a salt-water discrimination GO-NOGO task in monkeys

C.R. Plata-Salaman et al.

Gustatory neural coding in the monkey cortex: l-amino acids

J. Neurophysiol.

(1992)

T.S. Roberts et al.

Insular and opercular cortex and its thalamic projections in Macaca mulatta

Schwizer Arch. Neurol. Psychiatr.

(1963)

F. Sanides

The architecture of the cortical taste nerve areas in squirrel monkey (Saimiri sciureus) and their relationships to insular, sensorimotor and prefrontal regions

Brain Res.

(1968)

C.B. Saper

J. Neurophysiol.

(1985)

A. Adler

Zur Topik der corticalen Geschmackssphäre

Zeitschr. Neur. Psych.

(1935)

M.H. Bagshaw et al.

Cortical organization in gustation (Macaca mulatta)

J. Neurophysiol.

(1953)

R.M. Beckstead et al.

The nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei

J. Comp. Neurol.

(1980)

W.S. Bornstein

Cortical representation of taste in man and monkey. I. Functional and anatomical relations of taste, olfaction and somatic sensibility

Yale J. Biol. Med.

(1940)

W.S. Bornstein

Cortical representation of taste in man and monkey. II. The localization of the cortical taste area in man and a method of measuring impairment of taste in man

Yale J. Biol. Med.

(1940)

W.H. Bradley

Central localization of gustatory perception: an experimental study

J. Comp. Neurol.

(1963)

H. Burton et al.

Central projections of the gustatory system

H. Burton et al.

The posterior thalamic region and its cortical projection in New World and Old World monkeys

J. Comp. Neurol.

(1976)

S.T. Carmichael et al.

Convergent olfactory, taste/visceral, and other sensory inputs to the monkey orbital cortex

M.J. Cohen et al.

Cortical reception of touch and taste in the cat

Acta Physiol. Scand.

(1957)

C.G. Cusick et al.

Somatotopic organization of the lateral sulcus of owl monkeys: area 3b, S-II, and a ventral somatosensory area

J. Comp. Neurol.

(1986)

D. Ferrier

The Croonian Lectures on Cerebral Localization

(1880)

O. Foerster

Sensible corticale Felder

M. Fujioka

Some observations of the projection to VPMpc from the so-called ‘frontal opercular pure taste area’

Appl. Neurophysiol.

(1976)

H. Fukuda et al.

High order gustatory projections in the human brain studied with positron emission tomography

J. Gad

Über Beziehungen des Grosshirns zum Fressakt beim Kaninchen

Du Bois Reymond's Arch. Physiol.

(1891)

M.A. Gerebtzoff

Les voies centrales de la sensibilité det du gout et leurs terminations thalamiques

Cellule

(1939)

M.A. Gerebtzoff

Recherches oscillographiques et anatomophysiologiques sur les centres cortical et thalamique du gout

Arch. intern. Physiol.

(1941)

E. Gerhardt

Der Isocortex parietalis beim Schimpanzen

J. Psychol. Neurol. (Lpz)

(1938)

Dr. Gorschkow

Ueber Geschmacks- und Geruchszentrum in der Hirnrinde, Inaugural dissertation

(1901)

Abstr. Neurol. Zentralbl., 20:...

C. Hausser-Hauw et al.

Gustatory hallucinations in epileptic seizures. Electrophysiological, clinical and anatomical correlates

Brain

(1987)

G. Hellekant et al.

Single taste fibers in chimpanzee and rhesus monkey

S. Ito et al.

Unit activities of fronto-opercular cortex in the macaque monkeys performing a gustatory GO/NOGO task

J. Physiol. Soc. Jpn.

(1988)

S. Ito et al.

Neural activities in the fronto-opercular cortex of macaque monkeys during tasting and mastication

Jpn. J. Physiol.

(1994)

J.Hughlings Jackson

Lectures on the diagnosis of epilepsy

E.G. Jones et al.

Areal differences in the distribution of thalamic afferents in the insular, parietal and temporal regions of primates

J. Comp. Neurol.

(1976)

E.A. Kahn et al.

Correlative Neurosurgery

(1969)

T. Kusama et al.

Stereotaxic Atlas of the Brain of Macaca fuscata

(1970)

Cited by (108)

Making developmental sense of the senses, their origin and function
2024, Current Topics in Developmental Biology
The primary senses—touch, taste, sight, smell, and hearing—connect animals with their environments and with one another. Aside from the eyes, the primary sense organs of vertebrates and the peripheral sensory pathways that relay their inputs arise from two transient stem cell populations: the neural crest and the cranial placodes. In this chapter we consider the senses from historical and cultural perspectives, and discuss the senses as biological faculties. We begin with the embryonic origin of the neural crest and cranial placodes from within the neural plate border of the ectodermal germ layer. Then, we describe the major chemical (i.e. olfactory and gustatory) and mechanical (i.e. vestibulo-auditory and somatosensory) senses, with an emphasis on the developmental interactions between neural crest and cranial placodes that shape their structures and functions.
Functional characterization of macaque insula using task-based and resting-state fMRI
2023, NeuroImage
Neurophysiological investigations over the past decades have demonstrated the involvement of the primate insula in a wide array of sensory, cognitive, affective and regulatory functions, yet the complex functional organization of the insula remains unclear. Here we examined to what extent non-invasive task-based and resting-state fMRI provides support for functional specialization and integration of sensory and motor information in the macaque insula. Task-based fMRI experiments suggested a functional specialization related to processing of ingestive/taste/distaste information in anterior insula, grasping-related sensorimotor responses in middle insula and vestibular information in posterior insula. Visual stimuli depicting social information involving conspecific`s lip-smacking gestures yielded responses in middle and anterior portions of dorsal and ventral insula, overlapping partially with the sensorimotor and ingestive/taste/distaste fields. Functional specialization/integration of the insula was further corroborated by seed-based whole brain resting-state analyses, showing distinct functional connectivity gradients across the anterio-posterior extent of both dorsal and ventral insula. Posterior insula showed functional correlations in particular with vestibular/optic flow network regions, mid-dorsal insula with vestibular/optic flow as well as parieto-frontal regions of the sensorimotor grasping network, mid-ventral insula with social/affiliative network regions in temporal, cingulate and prefrontal cortices and anterior insula with taste and mouth motor networks including premotor and frontal opercular regions.
Infection, learning, and memory: Focus on immune activation and aversive conditioning
2022, Neuroscience and Biobehavioral Reviews
Here we review the effects of immune activation primarily via lipopolysaccharide (LPS), a cell wall component of Gram-negative bacteria, on hippocampal and non-hippocampal-dependent learning and memory. Rodent studies have found that LPS alters both the acquisition and consolidation of aversive learning and memory, such as those evoking evolutionarily adaptive responses like fear and disgust. The inhibitory effects of LPS on the acquisition and consolidation of contextual fear memory are discussed. LPS-induced alterations in the acquisition of taste and place-related conditioned disgust memory within bottle preference tasks and taste reactivity tests (taste-related), in addition to conditioned context avoidance tasks and the anticipatory nausea paradigm (place-related), are highlighted. Further, conditioned disgust memory consolidation may also be influenced by LPS-induced effects. Growing evidence suggests a central role of immune activation, especially pro-inflammatory cytokine activity, in eliciting the effects described here. Understanding how infection-induced immune activation alters learning and memory is increasingly important as bacterial and viral infections are found to present a risk of learning and memory impairment.
Laser stimulation of the skin for quantitative study of decision-making and motivation
2022, Cell Reports Methods
Citation Excerpt :
However, it remains unclear whether other decision-related attributes, such as the magnitude of noxious stimuli, are reflected in the activity of OFC neurons signaling reward value during the decision process. Anatomical studies suggest that the OFC is positioned as a second-order gustatory cortex (Lara et al., 2009; Ogawa, 1994; Ongur and Price, 2000; Rolls and Baylis, 1994; Seabrook and Borgland, 2020; Sewards and Sewards, 2001) that could, in principle, be explicitly dedicated to processing the value of primary consumptive reward. In contrast to this idea, human imaging studies indicate that the OFC is sensitive to financial and abstract rewards (Charpentier et al., 2018; Kahnt et al., 2010; O'Doherty et al., 2001).
Neuroeconomics studies how decision-making is guided by the value of rewards and punishments. But to date, little is known about how noxious experiences impact decisions. A challenge is the lack of an aversive stimulus that is dynamically adjustable in intensity and location, readily usable over many trials in a single experimental session, and compatible with multiple ways to measure neuronal activity. We show that skin laser stimulation used in human studies of aversion can be used for this purpose in several key animal models. We then use laser stimulation to study how neurons in the orbitofrontal cortex (OFC), an area whose many roles include guiding decisions among different rewards, encode the value of rewards and punishments. We show that some OFC neurons integrated the positive value of rewards with the negative value of aversive laser stimulation, suggesting that the OFC can play a role in more complex choices than previously appreciated.
Neural encoding of food and monetary reward delivery
2022, NeuroImage
Different types of rewards such as food and money can similarly drive our behavior owing to shared brain processes encoding their subjective value. However, while the value of money is abstract and needs to be learned, the value of food is rooted in the innate processing of sensory properties and nutritional utilization. Yet, the actual consumption of food and the receipt of money have never been directly contrasted in the same experiment, questioning what unique neural processes differentiate those reward types. To fill this gap, we examined the distinct and common neural responses to the delivery of food and monetary rewards during fMRI.
In a novel experimental approach, we parametrically manipulated the subjective value of food and monetary rewards by modulating the quantities of administered palatable milkshake and monetary gains. The receipt of increasing amounts of milkshake and money recruited the ventral striatum and the ventromedial prefrontal cortex, previously associated with value encoding. Notably, the consumption and the subsequent evaluation of increasing quantities of milkshake relative to money revealed an extended recruitment of brain regions related to taste, somatosensory processing, and salience. Moreover, we detected a decline of reward encoding in the ventral tegmental area, nucleus accumbens, and vmPFC, indicating that these regions may be susceptible to time-dependent effects upon accumulation of food and money rewards.
Relative to monetary gains, the consumption and evaluation of palatable milkshakes engaged complex neural processing over and above value tracking, emphasizing the critical contribution of taste and other sensory properties to the processing of food rewards. Furthermore, our results highlight the need to closely monitor metabolic states and neural responses to the accumulation of rewards to pinpoint the mechanisms underlying time-dependent dynamics of reward-related processing.
Beyond language: The unspoken sensory-motor representation of the tongue in non-primates, non-human and human primates
2022, Neuroscience and Biobehavioral Reviews
The English idiom “on the tip of my tongue” commonly acknowledges that something is known, but it cannot be immediately brought to mind. This phrase accurately describes sensorimotor functions of the tongue, which are fundamental for many tongue-related behaviors (e.g., speech), but often neglected by scientific research. Here, we review a wide range of studies conducted on non-primates, non-human and human primates with the aim of providing a comprehensive description of the cortical representation of the tongue’s somatosensory inputs and motor outputs across different phylogenetic domains. First, we summarize how the properties of passive non-noxious mechanical stimuli are encoded in the putative somatosensory tongue area, which has a conserved location in the ventral portion of the somatosensory cortex across mammals. Second, we review how complex self-generated actions involving the tongue are represented in more anterior regions of the putative somato-motor tongue area. Finally, we describe multisensory response properties of the primate and non-primate tongue area by also defining how the cytoarchitecture of this area is affected by experience and deafferentation.

View all citing articles on Scopus

View full text

Review articleGustatory cortex of primates: anatomy and physiology

Abstract

Physiol. Behav.

Brain Res.

Brain Res.

Neurosci. Lett.

Behav. Brain Res.

J. Neurosci.

Neurosci. Res.

Neurosci. Res.

J. Neurophysiol.

Schwizer Arch. Neurol. Psychiatr.

Brain Res.

J. Neurophysiol.

Zur Topik der corticalen Geschmackssphäre

Zeitschr. Neur. Psych.

Cortical organization in gustation (Macaca mulatta)

J. Neurophysiol.

The nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei

J. Comp. Neurol.

Cortical representation of taste in man and monkey. I. Functional and anatomical relations of taste, olfaction and somatic sensibility

Yale J. Biol. Med.

Cortical representation of taste in man and monkey. II. The localization of the cortical taste area in man and a method of measuring impairment of taste in man

Yale J. Biol. Med.

Central localization of gustatory perception: an experimental study

J. Comp. Neurol.

Central projections of the gustatory system

The posterior thalamic region and its cortical projection in New World and Old World monkeys

J. Comp. Neurol.

Convergent olfactory, taste/visceral, and other sensory inputs to the monkey orbital cortex

Cortical reception of touch and taste in the cat

Acta Physiol. Scand.

Somatotopic organization of the lateral sulcus of owl monkeys: area 3b, S-II, and a ventral somatosensory area

J. Comp. Neurol.

The Croonian Lectures on Cerebral Localization

Sensible corticale Felder

Some observations of the projection to VPMpc from the so-called ‘frontal opercular pure taste area’

Appl. Neurophysiol.

High order gustatory projections in the human brain studied with positron emission tomography

Über Beziehungen des Grosshirns zum Fressakt beim Kaninchen

Du Bois Reymond's Arch. Physiol.

Les voies centrales de la sensibilité det du gout et leurs terminations thalamiques

Cellule

Recherches oscillographiques et anatomophysiologiques sur les centres cortical et thalamique du gout

Arch. intern. Physiol.

Der Isocortex parietalis beim Schimpanzen

J. Psychol. Neurol. (Lpz)

Ueber Geschmacks- und Geruchszentrum in der Hirnrinde, Inaugural dissertation

Gustatory hallucinations in epileptic seizures. Electrophysiological, clinical and anatomical correlates

Brain

Single taste fibers in chimpanzee and rhesus monkey

Unit activities of fronto-opercular cortex in the macaque monkeys performing a gustatory GO/NOGO task

J. Physiol. Soc. Jpn.

Neural activities in the fronto-opercular cortex of macaque monkeys during tasting and mastication

Jpn. J. Physiol.

Lectures on the diagnosis of epilepsy

Areal differences in the distribution of thalamic afferents in the insular, parietal and temporal regions of primates

J. Comp. Neurol.

Correlative Neurosurgery

Stereotaxic Atlas of the Brain of Macaca fuscata

Review article
Gustatory cortex of primates: anatomy and physiology